Centromere and telomere sequence alterations reflect the rapid genome evolution within the carnivorous plant genus Genlisea

Plant Journal

Volumn 84, Issue 6, 2015, Pages 1087-1099

  Tran, Trung D ^a   Cao, Hieu X ^a   Jovtchev, Gabriele ^a,e   Neumann, Pavel ^b   Novák, Petr ^b   Fojtová, Miloslava ^c   Vu, Giang T H ^a   MacAs, Jiří ^b   Fajkus, Jiří ^c,d   Schubert, Ingo ^a,c   Fuchs, Joerg ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b INSTITUTE OF PLANT MOLECULAR BIOLOGY   (Czech Republic)

^c MASARYK UNIVERSITY   (Czech Republic)

^d INSTITUTE OF BIOPHYSICS   (Czech Republic)

^e INSTITUTE OF BIODIVERSITY AND ECOSYSTEM RESEARCH   (Bulgaria)

Author keywords

centromeric retrotransposons; centromeric tandem repeat; G. hispidula; Genlisea nigrocaulis; genome evolution; Lentibulariaceae; plant telomeric repeat variants; telomerase

Indexed keywords

BIOLOGY; DNA SEQUENCES; GENES;

CENTROMERIC RETROTRANSPOSONS; G. HISPIDULA; GENLISEA NIGROCAULIS; GENOME EVOLUTION; LENTIBULARIACEAE; PLANT TELOMERIC REPEAT VARIANTS; TANDEM REPEATS; TELOMERASE;

CHROMOSOMES;

ANGIOSPERM; CENTROMERE; EVOLUTION; GENETIC VARIATION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT CHROMOSOME; PLANT GENOME; SPECIES DIFFERENCE; TELOMERE; TIME FACTOR;

ANGIOSPERMS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; CENTROMERE; CHROMOSOMES, PLANT; GENETIC VARIATION; GENOME, PLANT; MOLECULAR SEQUENCE DATA; SPECIES SPECIFICITY; TELOMERE; TIME FACTORS;

EID: 84946787990     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13058     Document Type: Article

References (51)

1. Adams, S.P., Leitch, I.J., Bennett, M.D., and, Leitch, A.R., (2000) Aloe L.-a second plant family without (TTTAGGG)n telomeres. Chromosoma, 109, 201-205.
2. Adams, S.P., Hartman, T.P., Lim, K.Y., Chase, M.W., Bennett, M.D., Leitch, I.J., and, Leitch, A.R., (2001) Loss and recovery of Arabidopsis-type telomere repeat sequences 5′-(TTTAGGG)(n)-3′ in the evolution of a major radiation of flowering plants. Proc. Biol. Sci. 268, 1541-1546.
3. Berr, A., Pecinka, A., Meister, A., Kreth, G., Fuchs, J., Blattner, F.R., Lysak, M.A., and, Schubert, I., (2006) Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. Plant J. 48, 771-783.
4. Cheng, Z., Dong, F., Langdon, T., Ouyang, S., Buell, C.R., Gu, M., Blattner, F.R., and, Jiang, J., (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell, 14, 1691-1704.
5. Demidov, D., Schubert, V., Kumke, K., et al. (2014) Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet. Genome Res. 143, 150-156.
6. Dong, Q., and, Han, F., (2012) Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. Plant J. 71, 800-809.
7. Dong, F., Miller, J.T., Jackson, S.A., Wang, G.-L., Ronald, P.C., and, Jiang, J., (1998) Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc. Natl Acad. Sci. USA, 95, 8135-8140.
8. Fajkus, J., Fulneckova, J., Hulanova, M., Berkova, K., Riha, K., and, Matyasek, R., (1998) Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol. Gen. Genet. 260, 470-474.
9. Fajkus, J., Sýkorová, E., and, Leitch, A.R., (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res. 13, 469-479.
10. Fitzgerald, M.S., McKnight, T.D., and, Shippen, D.E., (1996) Characterization and developmental patterns of telomerase expression in plants. Proc. Natl Acad. Sci. USA, 93, 14422-14427.
11. Fleischmann, A., (2012) Monograph of the Genus Genlisea: Redfern Natural History Productions.
12. Fleischmann, A., Michael, T.P., Rivadavia, F., Sousa, A., Wang, W., Temsch, E.M., Greilhuber, J., Muller, K.F., and, Heubl, G., (2014) Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. Ann. Bot. 114, 1651-1663.
13. Fojtova, M., Fulneckova, J., Fajkus, J., and, Kovarik, A., (2002) Recovery of tobacco cells from cadmium stress is accompanied by DNA repair and increased telomerase activity. J. Exp. Bot. 53, 2151-2158.
14. Fojtova, M., Wong, J.T.Y., Dvorackova, M., Yan, K.T.H., Sykorova, E., and, Fajkus, J., (2010) Telomere maintenance in liquid crystalline chromosomes of dinoflagellates. Chromosoma, 119, 485-493.
15. Fuchs, J., Brandes, A., and, Schubert, I., (1995) Telomere sequence localization and karyotype evolution in higher plants. Plant Syst. Evol. 196, 227-241.
16. Fukagawa, T., and, Earnshaw, W.C., (2014) The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell 30, 496-508.
17. Gong, Z.Y., Wu, Y.F., Koblizkova, A., et al. (2012) Repeatless and Repeat-Based Centromeres in Potato: implications for centromere evolution. Plant Cell, 24, 3559-3574.
18. Gorinsek, B., Gubensek, F., and, Kordis, D., (2004) Evolutionary genomics of chromoviruses in eukaryotes. Mol. Biol. Evol. 21, 781-798.
19. Greilhuber, J., Borsch, T., Worberg, A., Porembski, S., and, Barthlott, W., (2006) Smallest angiosperm genomes found in Lentibulariaceae, with chromosome of bacterial size. Plant Biol. 8, 770-777.
20. Henikoff, S., Ahmad, K., and, Malik, H.S., (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science, 293, 1098-1102.
21. Hosouchi, T., Kumekawa, N., Tsuruoka, H., and, Kotani, H., (2002) Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. DNA Res. 9, 117-121.
22. Houben, A., and, Schubert, I., (2003) DNA and proteins of plant centromeres. Curr. Opin. Plant Biol. 6, 554-560.
23. Houben, A., Brandes, A., Pich, U., Manteuffel, R., and, Schubert, I., (1996) Molecular-cytogenetic characterization of a higher plant centromere/kinetochore complex. Theor. Appl. Genet. 93, 477-484.
24. Houben, A., Wako, T., Furushima-Shimogawara, R., Presting, G., Kunzel, G., Schubert, I., and, Fukui, K., (1999) The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J. 18, 675-679.
25. Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R., and, Schubert, I., (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J. 33, 967-973.
26. Hudakova, S., Michalek, W., Presting, G.G., ten Hoopen, R., dos Santos, K., Jasencakova, Z., and, Schubert, I., (2001) Sequence organization of barley centromeres. Nucleic Acids Res. 29, 5029-5035.
27. Ibarra-Laclette, E., Lyons, E., Hernandez-Guzman, G., et al. (2013) Architecture and evolution of a minute plant genome. Nature, 498, 94-98.
28. Ijdo, J.W., Wells, R.A., Baldini, A., and, Reeders, S.T., (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 19, 4780.
29. Jiang, J., Birchler, J.A., Parrott, W.A., and, Dawe, R.K., (2003) A molecular view of plant centromeres. Trends Plant Sci. 8, 570-575.
30. Li, L., Yang, J., Tong, Q., Zhao, L., and, Song, Y., (2005) A novel approach to prepare extended DNA fibers in plants. Cytometry A, 63A, 114-117.
31. Lysak, M.A., Fransz, P., and, Schubert, I., (2006) Cytogenetic analyses of Arabidopsis. Methods Mol. Biol. 323, 173-186.
32. Ma, J., Wing, R.A., Bennetzen, J.L., and, Jackson, S.A., (2007) Plant centromere organization: a dynamic structure with conserved functions. Trends Genet. 23, 134-139.
33. Martinez-Zapater, J., Estelle, M., and, Somerville, C., (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol. Gen. Genet. 204, 417-423.
34. Melters, D., Bradnam, K., Young, H., et al. (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 14, R10.
35. Nasuda, S., Hudakova, S., Schubert, I., Houben, A., and, Endo, T.R., (2005) Stable barley chromosomes without centromeric repeats. Proc. Natl Acad. Sci. USA, 102, 9842-9847.
36. Neumann, P., Navratilova, A., Koblizkova, A., Kejnovsky, E., Hribova, E., Hobza, R., Widmer, A., Dolezel, J., and, Macas, J., (2011) Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mobile DNA, 2, 4.
37. Neumann, P., Navratilova, A., Schroeder-Reiter, E., Koblizkova, A., Steinbauerova, V., Chocholova, E., Novak, P., Wanner, G., and, Macas, J., (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet. 8, e1002777.
38. Novak, P., Neumann, P., and, Macas, J., (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics, 11, 378.
39. Peska, V., Fajkus, P., Fojtova, M., Dvorackova, M., Hapala, J., Dvoracek, V., Polanska, P., Leitch, A.R., Sykorova, E., and, Fajkus, J., (2015) Characterisation of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J. 82, 644-654.
40. Pich, U., and, Schubert, I., (1998) Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosome Res. 6, 315-321.
41. Pich, U., Fuchs, J., and, Schubert, I., (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res. 4, 207-213.
42. Plohl, M., Mestrovic, N., and, Mravinac, B., (2014) Centromere identity from the DNA point of view. Chromosoma, 123, 313-325.
43. Richards, E.J., and, Ausubel, F.M., (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell, 53, 127-136.
44. Sykorova, E., Lim, K.Y., Chase, M.W., Knapp, S., Leitch, I.J., Leitch, A.R., and, Fajkus, J., (2003a) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J. 34, 283-291.
45. Sykorova, E., Lim, K.Y., Fajkus, J., and, Leitch, A.R., (2003b) The signature of the Cestrum genome suggests an evolutionary response to the loss of (TTTAGGG)n telomeres. Chromosoma, 112, 164-172.
46. Sykorova, E., Lim, K.Y., Kunicka, Z., Chase, M.W., Bennett, M.D., Fajkus, J., and, Leitch, A.R., (2003c) Telomere variability in the monocotyledonous plant order Asparagales. Proc. Biol. Sci. 270, 1893-1904.
47. Sykorova, E., Fajkus, J., Meznikova, M., Lim, K.Y., Neplechova, K., Blattner, F.R., Chase, M.W., and, Leitch, A.R., (2006) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am. J. Bot. 93, 814-823.
48. Tran, T.D., Cao, H.X., Jovtchev, G., Novák, P., Vu, G.T.H., Macas, J., Schuber, I., and, Fuchs, J., (2015) Chromatin organization and cytological features of carnivorous Genlisea species with large genome size differences. Front. Plant Sci., 6, 613.
49. Veleba, A., Bures, P., Adamec, L., Smarda, P., Lipnerova, I., and, Horova, L., (2014) Genome size and genomic GC content evolution in the miniature genome-sized family Lentibulariaceae. New Phytol. 203, 22-28.
50. Vu, G.T., Schmutzer, T., Bull, F., et al. (2015) Comparative genome analysis revealed divergent genome size evolution in a carnivorous plant genus. Plant Genome, 8, 3.
51. Weiss, H., and, Scherthan, H., (2002) Aloe spp.-plants with vertebrate-like telomeric sequences. Chromosome Res. 10, 155-164.